J Mater Sci

Review
REVIEW

Zinc oxide nanoparticles: a review of their biological

synthesis, antimicrobial activity, uptake, translocation
and biotransformation in plants
Ajey Singh1 , N. B. Singh1,* , Shadma Afzal2 , Tanu Singh2 , and Imtiyaz Hussain1

1
Plant Physiology Laboratory, Department of Botany, University of Allahabad, Allahabad, India
2
Department of Botany, University of Allahabad, Allahabad, U.P. 211002, India

Received: 20 May 2017 ABSTRACT

Accepted: 31 August 2017 Over the past decade, incorporation of nanomaterials into agricultural practices
like nanofertilizers and nanopesticides has gained a lot of attention. Progress
Ó Springer Science+Business and application of fertilizers in nanoforms are one of the effective options for
Media, LLC 2017 considerable improvement of the agricultural yield worldwide. Zinc oxide
nanoparticles (ZnO NPs) are considered as a biosafe material for biological
species. Earlier studies have shown the potential of ZnO NPs in stimulation of
seed germination and plant growth as well as disease suppression and plant
protection by its antimicrobial activity. However, both positive and negative
effects of ZnO NPs on plant growth and metabolism at various developmental
periods have been documented. Uptake, translocation and accumulation of ZnO
NPs by plants depend upon the features of NPs as well as the anatomy of the
host plant. This review summarizes the applications of ZnO NPs as nanofer-
tilizer in crop production and also attempts to examine and record the possible
mechanism of antimicrobial activity of ZnO NPs. Biological synthesis of ZnO
NPs and their uptake, translocation and biotransformation in plants via various
routes have also been examined.

Introduction which can be defined as a small object that behaves as

a whole unit in terms of its transport and properties.
Nanotechnology provides a great possibility of novel Nanotechnology has a great potential to provide an
application in the fields of biotechnology and agri- opportunity for the researchers to develop new tools
cultural industries. It is the branch of technology that for incorporation of NPs into plants that could sup-
deals with materials having dimensions of less than plement existing functions and add new ones.
100 nanometers (nm), especially the manipulation of Interaction of NPs with plants causes several
discrete atoms and molecules [1]. Nanotechnology is morphological and physiological changes, depending
considered as the application of nanoparticles (NPs) on the properties of NPs. The efficiency of NPs is

Address correspondence to E-mail: [email protected]

DOI 10.1007/s10853-017-1544-1
 J Mater Sci

determined by different factors like their chemical microorganisms is emerging as a new area of interest
composition, size, surface covering, reactivity and nowadays. The biological approach to the synthesis
most importantly the extent to which they are effec- of NPs has an advantage over traditional chemical
tive [2]. Conventional fertilizers are being used and physical methods [13]. Applications of biosyn-
worldwide at high rates for augmentation in grain thesized metallic NPs range from various biomedical
production to fulfil the demand of the rapidly functions, viz. antimicrobial coatings, medical imag-
growing population. Even though fertilizers are cru- ing and drug delivery to catalytic water treatment
cial for plant growth and development, the majority and environmental sensors [6]. Green chemistry
of the applied fertilizers stay unavailable to plants reduces pollution risk at source level where the
due to numerous aspects and few of them are principle focus is on the choice of reagents which are
leaching, degradation by photolysis, hydrolysis and eco-friendly. In addition, Bioresource-based green
decomposition. Therefore, it is required to decrease synthesis of metal as well as metal oxide NPs has
the nutrient losses in fertilization and to improve the been reported [14]. Despite several advantageous
crop yield with the help of use of new techniques and aspects of ZnO NPs in agriculture sector, there are
their applications through nanotechnology and NPs. some reports discussing the toxicity of ZnO NPs on
Zinc (Zn) is the only metal found in all six enzyme plants. The annotation of mechanisms of cytotoxicity
classes, viz. oxidoreductases, lyases, isomerases, and genotoxicity of ZnO NPs remains an unexplored
transferases, hydrolases and ligases [3]. Zinc being field of study. The increasing commercial use and
essential micronutrient plays an important role in extensive fabrication of engineered NPs may result in
many integral metabolic processes [4]. Zn can also help unintended exposure to flora and fauna of the envi-
increase the biosynthesis of chlorophylls and car- ronment. Key aspects that influenced toxicity in
otenoids and enhance the photosynthetic apparatus of plants are the concentration of NPs, particle size,
the plant [5]. Significant optoelectrical, physical and surface area, stability, physicochemical properties,
antimicrobial properties of zinc oxide (ZnO) NPs offers plant species, plant age/phenological stage, the
great potential to boost agriculture productivity [6]. medium of exposure and dilution agent [15]. It is
There are some studies which report strong absorption demonstrated that exposure of Allium cepa roots to
abilities for a series of organic compounds, heavy ZnO NPs causes cytotoxicity and genotoxicity [16]. In
metals, ZnO and its NPs [7]. ZnO NPs have a large another report, there was concentration-dependent
surface area-to-volume ratio that results in a signifi- inhibition of mitotic index, which indicated the
cant increase in the effectiveness in blocking UV radi- cytotoxic potential of ZnO NPs in Allium cepa [17].
ation as compared to the bulk material [8]. The major objective of this review is to collect,
The impact of ZnO NPs has been evaluated in vari- evaluate and create the most up to date knowledge
ous studies on crop plants. Nanodimensional ZnO regarding the biological synthesis of ZnO NPs and
particle enhanced germination, pigments, sugar and their role in improvement of plant growth and yield.
protein contents with increased activities of antioxi- This review also attempts to examine and record the
dant enzymes in various vegetable crops [9]. ZnO NPs possible mechanism of uptake, translocation and
have significant effect on the root epidermis and cortex accumulation of ZnO NPs in plants via different
of Lolium perenne with internalization of NPs in the routes. Moreover, this review is proposed to provide
endodermal and vascular tissues [10]. ZnO NPs pos- a critical assessment of the antimicrobial activity and
sess antimicrobial activity against many pathogenic phytotoxicity of the application of ZnO NPs in plants.
organisms like Escherichia coli, Pseudomonas aeruginosa,
Campylobacter jejuni. [11]. Increased yield is directly
linked to the decrease in number of pathogenic Biological synthesis of zinc oxide
microorganisms and also to the potential nutritional nanoparticles
value of the NPs themselves, mainly for the essential
micronutrients necessary for host defence [12]. Biological synthesis of NPs has an advantage over
ZnO NPs can be synthesized by several chemical conventional chemical and physical methods. In the
methods such as precipitation, vapour transport and recent times, ‘‘green’’ method for the synthesis of NPs
hydrothermal process. The biogenic synthesis of ZnO has become an area of utmost interest. The focus is
NPs by using different plant extracts or applied in this direction because the use of
J Mater Sci

Figure 1 Possible mechanism

involved in biological
synthesis of zinc oxide
nanoparticles.

conventional chemical methods is expensive and fields [19]. NPs synthesized by plants are more
requires the use of chemical compounds or organic stable and biocompatible due to the process of coat-
solvents as reducing agents [6]. Conventional chem- ing with biogenic surfactants or capping agents and
ical reduction method involves various toxic chemi- they also have reduced environmental impacts,
cals for the synthesis of NPs which can later be a exhibit variations in shape and size and have a faster
reason for various health issues due to their toxicity, rate of synthesis in comparison with the NPs pro-
while green synthesis method is an eco-friendly duced by other organisms [19]. The faster rate of
approach to produce NPs. Green synthesis method is synthesis is owed to the biological capacity to act as a
free of contaminants thus favorable for biological catalyst for reactions in aqueous media at standard
applications where purity is a matter of concern [18]. temperature and pressure conditions [6].
The use of toxic chemicals on the surface of NPs and A diagrammatic representation summarizing the
non-polar diluents in the chemical synthesis method possible mechanism of biological synthesis of ZnO
restricts their applications in clinical and biological NPs is given in Fig. 1. In biological synthesis of NPs,
 J Mater Sci

Table 1 Biological synthesis of zinc oxide nanoparticles using different biological extracts

Biological entities Precursor conditions Shape Size (nm) References

Aeromonas Hydrophila ZnO, 24 h at 30 °C Spherical and oval 57.72 [20]

Aloe barbadensis (source gel) Zn(NO3)2, 5–6 h at 150 °C Spherical 40 [25]
Cassia auriculata (flower extract) ZnNO3, 60–80 °C Spherical [26]
Hibiscus subdariffa (leaf extract) Zn(CH3COO)2H2O [27]
Coriandrum sativum (leaf extract) Zn(O2CCH3)2(H2O)2, [22]
overnight at 60 °C
Calotropis gigantea (leaf extract) ZnNO3, 60–400 °C Spherical-shaped 30–35 [22]
forming
agglomerates
Calotropis procera (latex) Zn(CH3COO)2H2O, Spherical and granular 5–40 [28]
NaOH, 60 °C nature
Acalypha indica (leaf extract) Zn(O2CCH3)2(H2O)2, [23]
overnight at 60 °C
Catharanthus roseus (leaf extract) Zn(CH3COO)2H2O, Spherical 23–57 [21]
NaOH
Elaeagnus angustifolia (flower extract) Zn(CH3COO)2H2O, Spherical 20–40 [7]
NaOH
Rhizoctonia bataticola ZnO salt solution Spherical 15–25 [29]
Aspergillus fumigatus, Aspergillus ZnSO4, ZnO, ZnCl2 and Oval to spherical 30–70 [30]
flavus (extracellular secretions) ZnNO3
Camellia sinensis (aqueous extract of Zn(CH3COO)2H2O, 16 [31]
green tea leaves) overnight dried at 60 °C
Hibiscus rosa sinensis (leaf extract) ZnNO3 Spherical and 30–35 [32]
crystalline
Citrus aurantifolia (fruit extract) Zn(CH3COO)2H2O Spherical 50–200 [33]
Lobelia leschenaultiana (leaf extract) Zn(O2CCH3)2 Spherical and 20–65 [34]
hexagonal
Abrus precatorius (aqueous solution of Zn(CH3COO)2H2O Spherical 90–500 [35]
seed extract)
Alternaria alternata ZnSO4 Spherical, triangular 45–150 nm with average [36]
and hexagonal size of 75 ± 5 nm
Plectranthus amboinicus (leaf extract) ZnO salt solution, 80 °C Rod shaped 50–180 [37]
for 5 h
Azadirachta indica (leaf extract) Zn(CH3COO)22H2O Spherical 9.6–25.5 [38]
Ixora coccinea (leaf extract) Zn(CH3COO)2H2O Spherical 145.1 [39]
Poncirus trifoliata (leaf extract) ZnNO3 Nearly spherical 8.48–32.5 [40]
Lantana aculeata (leaf extract) ZnNO3 Spherical 12 ± 3 [41]
Sargassum myriocystum (sea weed ZnNO3 Hexagonal, triangular, 36 [42]
extract) rod and radial
Parthenium hysterophorus (leaf ZnNO3 Spherical, hexagonal 27 ± 5, 84 ± 2 [43]
extract)
Sedum alfrediihance ZnNO3 Pseudo spherical 53.7 [44]

the plant/microorganism extract is simply mixed extracts and few reproducible microorganisms as
with a metal salt solution at room temperature. The eco-friendly reducing and capping agents.
synthesis process completes within hours. There are Synthesis of ZnO NPs (57–72 nm, spherical), via
plenty of reports on the green synthesis of ZnO NPs. reproducible bacteria Aeromonas hydrophila was car-
This report embodies some studies dealing with the ried out at room temperature from ZnO solution in a
biosynthesis of ZnO NPs using different plant duration of 24 h. The synthesized NPs exhibited
antimicrobial activity against both Pseudomonas
J Mater Sci

aeruginosa and Aspergillus flavus [20]. Extracellular been performed up to germination stage, providing
synthesis of ZnO NPs (23–57 nm, spherical) was only limited information and the results obtained are
carried out by reduction of 0.025 M aqueous zinc sometimes contradictory. One of the most important
acetate with an aqueous leaf extract of Catharanthus factors for uptake is the size of NPs, and it is prob-
roseus. These ZnO NPs were evaluated for antibac- lematic for NPs of large size to enter through the
terial activity, and the maximum antimicrobial plant cell walls and transport across the plasma
activity was recorded against Pseudomonas aeruginosa membranes. Ions and water can move easily through
followed by Staphylococcus aureus [21]. ZnO NPs ion channels and aquaporins, respectively, because
(20–40 nm) were rapidly synthesized at room tem- the size of ions and water molecules are around
perature by treating zinc acetate dehydrate with the 0.28 nm, whereas the cell wall pore size fluctuates in
flower extract of Elaeagnus angustifolia [7], and these between 2 and 20 nm [48]. The surface characteristics
synthesized particles reflected the positive effect on of NPs are also important for their aggregation pat-
growth and metabolism of tomato plant at low con- tern, movement in aquatic and terrestrial ecosystems
centration. The synthesis of ZnO NPs by reduction of and interactions with algae, plants and fungi [49].
aqueous zinc acetate dehydrate using leaf extract of Uptake and accumulation of ZnO NPs (8 nm) by
Coriandrum sativum, Calotropis gigantea and Acalypha Glycine max seedlings were examined by Lopez-
indica was also reported [22, 23]. The synthesis Moreno [50]. The Zn uptake by soybean seedlings
mechanism of ZnO NPs is a complicated process and was higher at 500 mg L-1 due to lesser aggregation,
not explored in detail. In the biological synthesis whereas, at high concentrations (1000–4000 mg L-1),
process, ZnO produced due to reaction between an increased chance for aggregate formation was
Zn?? ions coming from zinc salt and reducing agent proposed, making passage difficult through the cell
which can be a biological extract. Various phyto- wall pores consequently, reducing Zn uptake and
chemicals viz., polyphenols, carboxylic acid, amino accumulation. Although it is expected that ZnO NP is
acids and proteins, might act as stabilizing or growth a source for Zn2? found within tissues but the results
terminator of ZnO NPs as well as a linker molecule in X-ray absorption spectroscopy (XAS) study fail to
between two or more ZnO NPs in making self- figure out the source of Zn2? whether it is produced
assembly [7, 24]. by the biotransformation of the ZnO NP or not.
Table 1 summarizes some of the reports pertaining Therefore, it can be concluded that ZnO NPs ionized
to the synthesis of NPs mediated by the different by the root exudates on the root surface, as no trace of
biological extracts. ZnO NPs was found in XAS spectra. Similarly, in
ryegrass (Lolium perenne), SEM and TEM analyses
reveal the presence of ZnO NPs scattered in the
Uptake, translocation and accumulation apoplast, cytoplasm, nuclei of the endodermal cells
of zinc oxide nanoparticles and the vascular cylinder of the plant [10]. However,
results of the study were contradicted by the findings
Transport of NPs through environment into the of Wang P et al. [45] which shows that there was no
plants is the most critical factor to estimate NPs translocation detected from root to shoot in the Vigna
impact on plant metabolism. Plants are an essential unguiculata plant, in spite of extensive quantity of
component of the environment and act as a probable NPs around the root surface. Hence the Zn transfer
pathway for the uptake, transport and accumulation coefficient which is the fraction of Zn in the leaf
of NPs into the food chain [45]. Uptake, translocation comparative to the root was quite low. Therefore,
and accumulation of NPs depend on the plant species restricted transport of ZnO NPs to the shoot or its
and the size, chemical configuration, stability and increased adhesion might be the reason of increased
concentration of the NPs. The high mobility of NPs is accumulation of Zn in roots. On exposure to the
determined by van der Waal forces, Brownian motion environment, ZnO NPs rapidly undergo dissolution
(diffusion), gravity and double-layer forces which are or biotransformation and the attachment of NPs to
responsible for their adhering property [46, 47]. The the soil particles also explains the absence of ZnO
processes of translocation and accumulation of ZnO NPs in shoots [51, 52]. Carboxyl groups play a sig-
NPs in crops are not studied adequately. This area of nificant role as ligands involved in the transport and
research is recent and the studies have commonly storage of Zn in shoots [53]. In the seeds of Vigna
 J Mater Sci

(a) Foliar Entry through wound Aggregaon on leaf epidermis Entry through
exposure hydathodes

Entry through cucle penetraon Entry through stomata

(b) Root Symplasc pathway

exposure
Through injury
Soil parcles

Entry through lencel

Apoplasc pathway

Biotransformaon

ZnO NPs Zn2+ ZnPO4

Figure 2 An overview and general principle of uptake, translo- hydathodes and wounds. b Transverse cross section of the root
cation and biotransformation pathway of zinc oxide nanoparticles showing entry of nanoparticles through lenticels, injury or
in a plant system. a Transverse cross section of the leaf showing biotransformation into zinc ions and they follow apoplastic and
entry of nanoparticles through stomata, cuticle penetration, symplastic pathways.

unguiculata, high concentration of Zn was reported in division and elongation of the root tips, and hence the
the outer layer of cotyledon and hypocotyl, while low ZnO NPs were detected mainly in the epidermis,
Zn concentration in the testa and inner cotyledon. cortex, vascular system and root tip cells. ZnO NPs
LCF examination of seeds indicated that Zn was enter the vascular system through the gaps of the
predominantly associated with citrate, histidine, casparian strips at the location of the primary and
malate, phytate and polygalacturonic acid and pre- lateral root junction but no ZnO NPs were observed
cipitated in the form of zinc phosphate [45]. to be translocated into shoots, possibly due to the
In recent study, Jitao et al. [54] investigated that a dissolution and biotransformation of ZnO NPs inside
large amount of Zn was taken up resulting from Zn2? the plants from ZnO NPs to ZnPO4 which further
released from ZnO NPs and Zn accumulated in the limit their long-distance transport. The use of confo-
form of ZnPO4ZnO NPs adsorbed on root surfaces cal microscopy technique suggested the uptake of
move into the root cortex as a result of quick cell ZnO NPs in corn plants growing in soil [55]. It was
J Mater Sci

observed that aggregates of ZnO NPs entered the concentration of 500 mg kg-1 of ZnO NPs resulted in
root epidermis and cortex via the apoplastic path- an increase in lateral root production while those in
way. However, the occurrence of ZnO NPs aggre- the acidic soil decreased root growth.
gates in xylem vessels in corn proposed the Exogenously synthesized ZnO NPs using extra-
movement through the symplastic pathway via the cellular secretions of Aspergillus fumigatus affected
endodermis. A schematic representation is given to Cyamopsis tetragonoloba when applied by foliar treat-
demonstrate the pathway for uptake, translocation ment [61]. Shoot length (22.7%), root length (43.4%),
and accumulation of zinc in the form of ZnO NPs and total protein content (17.2%), chlorophyll content
zinc ions in plant; for detailed understanding, the (54.5%) and rhizosphere microbial population
transverse cross section of leaf and root is shown to (13.6%) increased significantly. A similar observation
display possible pathways and mechanisms of has been recorded on the growth of Pennisetum
absorption, translocation and biotransformation of americanum using Zn NP (10 mg L-1) biosynthesized
ZnO NPs (Fig. 2). by Rhizoctonia bataticola [29].
Raliya et al. [59] studied the influence of ZnO NPs
(25 ± 3.5 nm) on the tomato plant. The authors con-
Zinc oxide nanoparticles as biofertilizer sidered parameters such as plant life cycle, fruit
yield, total biomass, nutritive value and chlorophyll
Zn deficiency is the most common micronutrient contents. The results from the study specified an
deficiency confining crop production in the world optimum concentration of ZnO NPs which promoted
[56]. Studies have successfully demonstrated that the the plant development while no stimulation was
nanopowders can be effectively used as fertilizers reported beyond the optimum concentration. The
[57]. ZnO NPs have potential to increase the yield foliar application was more effective than soil treat-
and growth of food crops. The use of ZnO NPs as a ments. The authors reported that the highest stimu-
Zn fertilizer in soil and also as a foliar fertilizer has lation in plant height, root length and biomass was
been proposed [58]. observed at a concentration of 250 mg kg-1, whereas
Apart from the property of rapid absorption, the maximum lycopene content and fruit yield at
nanofertilizers also exhibit slow release and they are 100 mg kg-1 and improved chlorophyll content at
required in scarce amount and thus can reduce fer- 750 mg kg-1 concentration.
tilizer consumption and environmental pollution The seeds of Arachis hypogea treated with different
[57]. ZnO NP apart from being an essential concentrations of ZnO NPs (25 nm) affected the plant
micronutrient is also a co-factor for nutrient mobi- growth factors such as seed germination, seedling
lizing and activating enzymes [59]. It is essential to vigour index, root growth, flowering, chlorophyll
mention that selection of the suitable concentration of content and pod yield [62]. It has been reported that
NPs is vital for obtaining higher profits for an aimed ZnO NPs at a concentration of 1000 ppm promoted
agro-economic attribute [59]. The equation given seed germination as well as seedling vigour and
below refers basically to the dissolution of ZnO NPs increased stem and root growth. The early germina-
into soluble ions in solution (water or soil solutions) tion and establishment of seeds in soil resulted in
causing discharge of the micronutrient (Zn). The early flowering and increased chlorophyll content in
amount and speed of dissolution are considerably leaf.
higher than bulk fertilizers due to the reduced par- ZnO NPs (15–40 nm) were synthesized using the
ticle size and greater specific surface area of ZnO flower extract of Elaeagnus angustifolia [7]. The effect
NPs. of different concentrations of ZnO NPs and zinc
ZnO(NPs) þ H2 O , Zn2þ þ 2OH sulphate (ZnSO4) on Solanum lycopersicum was
reported. The authors observed an increase in ger-
Triticum aestivum grown in acidic and alkaline soils mination rate, seedling vigour, pigment, protein and
amended with ZnO NPs exhibited 200 times higher sugar content at a concentration of 1.2 mM with
soluble Zn content in the acidic soil and ten times respect to control and ZnSO4ZnO NPs in 3.0 mM
higher concentration of Zn in wheat shoots, com- concentration successfully decreased the MDA and
pared to the alkaline soil [60]. On the other hand, SOD contents. Leaves of plants exposed to 6.1 mM
plants grown in the alkaline soil amended with a concentration of ZnO NPs recorded utmost
 J Mater Sci

Table 2 Positive impact of zinc oxide nanoparticles in different plant species

NPs Size Concentrations Test plants Effects References

(nm)

ZnO 800 mg kg-1 Cucumis sativus Enhanced growth and increase in dry weight [66]
NPs (fruit)
ZnO 25 1000 ppm (foliar Arachis hypogaea Increased germination, chlorophyll, stem and root growth [62]
NPs spray) and pod yield (29.5%)
ZnO 500, 1000, 2000 and Vigna radiata Increase in dry weight [67]
NPs 4000 ppm
ZnO 1 mg L-1 Cicer arietinum Increase in shoot height (6%), shoot biomass (27%), root [68]
NPs (chickpea seedlings) length (53%) and root biomass (37%)
ZnO 2 mg L-1 Brassica napus (rape Root elongation and increased seed germination [69]
NPs seed)
ZnO 1.5 ppm (foliar Cicer arietinum L var. Increase in shoot dry weight [70]
NPs spray) HC-1
ZnO 20 mg L-1 Vigna radiata (mung Increase in shoot height (98%) shoot biomass (76%), root [68]
NPs bean) length (42%) and root biomass (41%)
ZnO 2 mg L-1 Lolium perenne Enhanced growth of seedlings and root elongation [69]
NPs (ryegrass seed)
ZnO 20 ppm Vigna radiata Increase in biomass [71]
NPs (suspension, foliar
spray)
ZnO 2 ppm Zea mays corn (SC Increase in shoot dry matter and leaf area index by 63.8 [72]
NPs 704) and 69.7%
ZnO 1.2–6.8 10 ppm Cyamopsis Increased biomass, root and shoot length, chlorophyll [61]
NPs tetragonoloba content and protein synthesis
ZnO 60 mg L-1 Lupinus termis Decreased MDA and Na content, improved salt tolerance [73]
NPs in plant
ZnO 20–50 1000 mg L-1 Triticum aestivum Increased pigment and protein content [26]
NPs (wheat)
ZnO 2 mg L-1 Raphanus sativus Improved root elongation in germinated seeds [69]
NPs (radish)
ZnO 500 mg L-1 Glycine max Increased root growth [50]
NPs (soybean)
ZnO 20 20 lg mL-1 Allium cepa (onion) Increased seed germination [74]
NPs
Zn 15–25 10 mg L-1 Pennisetum glaucum Enhanced shoot (10.8%), chlorophyll content (18.4%) and [29]
NPs (pearl millet) grain yield (29.5%)
ZnO [100 10 mg L-1 Brassica nigra (black Shoot emergence, root hair formation and enhanced radical [75]
NPs mustard) scavenging activity
ZnO 9 lM Cabbage, cauliflower Increased pigment and protein content [9]
NPs and tomato

reflectance. In the study of Ates et al. [63], it has been Some of the applications reported in this review are
reported that the suspensions of Zn NPs induced summarized in Table 2 which shows examples taking
more toxicity than ZnO NPs to Artemia salina larvae. into account of the ZnO NPs, their size and concen-
Authors of this study concluded that this effect was tration, the plant species and the observed positive
associated with prominent release of free Zn2? from effects. Peng et al. [64] reported that aggregation and
Zn NPs into exposure medium. Moreover, both Zn dissolution of NPs and ROS generation by NPs can be
and ZnO NPs exhibited differences in toxic impacts influenced by many factors, including the size,
depending on the size of their nanopowders, viz. the shapes and surface charge of NPs. The shape of NPs
smaller size NPs were found to be more toxic. can affect both the equilibrium concentrations and
J Mater Sci

Figure 3 Possible affirmative

and negative impacts of zinc
oxide nanoparticles on plant
growth and metabolism.

rates of their dissolution. In the study of Misra et al. the ability to absorb UV radiation [79]. There are
[65], it was reported that the dissolved rate of numerous reports stating that Gram-positive bacteria
spherical NPs was faster than that of rod and spindle- are probably extra sensitive to ZnO NPs than Gram-
shaped NPs. negative bacteria [38]. In this report, we have conferred
Figure 3 shows some of the positive and negative various studies that described the antimicrobial effect
effects of ZnO NPs as fertilizer in agricultural crops of ZnO NPs on various microbes (Table 3).
as reported by various researchers. ZnO NPs have ZnO NPs (9.6–25.5 nm, spherical) synthesized via
both positive and negative impacts on germination, Azadirachta indica (neem) leaf extract have been used
growth, biomass, leaf area, radical scavenging activ- for their high antibacterial impact. The study repor-
ity, shoot and root length, protein content, photo- ted the antibacterial activity of ZnO NPs against
synthetic pigments and yield. Staphylococcus aureus, Streptococcus pyogenes and
Escherichia coli at wide range of concentration. The
percentage of bacterial growth reduction was found
Antimicrobial activity of zinc oxide to be 69.2, 57 and 52% for E. coli, S. aureus and S.
nanoparticles pyogenes, respectively [38].
ZnO NPs can inhibit and destroy food-borne
Vigneshwaran et al. [76] were the first to publish pathogens [80, 81]. In the report of Kaur et al. [80], the
reports on antimicrobial effects of biosynthesized NPs. bactericidal activity of ZnO NPs (8–10 nm) against
These NPs exhibit antifungal, anticorrosive, antibac- E. coli DH5a and S. Aureus was effective at 80 and
terial properties due to increased specific surface area, 100 gm L-1. ZnO NPs disordered and degenerated
reduced particle size, enhanced particle surface reac- the cell membrane of bacteria causing cytoplasmic
tivity and abrasive surface texture or surface defects leakage. The NPs which act as bactericidal agents on
[77]. ZnO NPs have recently shown to provide effec- the food surface where bacteria reside, hinder the
tive pathogen growth control as they have lower tox- growth of bacteria thus preventing food spoilage [82].
icity as well as positive impact on soil fertility [78]. The This type of packaging is called antimicrobial pack-
chemically synthesized ZnO NPs have been found to aging, where direct interaction occurs between the
be convincing antibacterial agents because they have product and the NPs leading to the killing or
 J Mater Sci

Table 3 Antimicrobial activity of zinc oxide nanoparticles

NPs and Growth media Pathogens Effects References

concentrations

ZnO NPs Culture Escherichia coli and Inhibition in growth of bacterial cell [90]
Staphylococcus aureus
ZnO NPs Culture Mucor plumbeus Inhibition of spore germination [91]
100 mg L-1
ZnO NP Mung bean Fusarium graminearum Reduced growth 26% [92]
broth agar
ZnO NPs Culture Pseudomonas aeruginosa High suppression in growth [20]
25 lg mL-1
ZnO NPs Plating assay Botrytis cinerea and Inhibited growth (63–80%) and (61–91%), respectively, [93]
3–12 mM Penicillium expansum hyphal malformation and fungal death
ZnO NPs Soil Pseudomonas putida Beneficial effect [90]
ZnO NPs Culture Klebsiella pneumoniae Inhibitory effect [31]
ZnO NPs Plating assay Fusarium oxysporum 20% decrease in fungal germination and 15% reduction in [94]
hyphal growth
ZnO NPs Culture media Listeria monocytogenes Growth inhibition [95]
10 mM and milk and Bacillus cereus

inhibition of bacterial growth on food surface [83]. was tested against P. aeruginosa ATCC 6749, S. aureus
ZnO NPs (36 nm) have been synthesized using Sar- ATCC 4163, E. coli ATCC 25922, S. Aureus and P.
gassum myriocystum (brown seaweed) [42]. The aeruginosa. The synthesized ZnO NPs exhibited high
authors reported that ZnO NPs exhibited moderate activity against S. Aureus ATCC 4163, E. coli ATCC
activity against Gram-positive bacteria like Strepto- 25922, S. aureus at 1028 lg mL-1 and maximum zone
coccus mutants, Vibrio cholerae and Neisseria gonorrhoea of their growth inhibition was 31 mm, while in P.
and low activity against Gram-negative bacteria such aeruginosa and P. aeruginosa ATCC 6749 high activity
as Micrococcus luteus and Klebsiella pneumoniae. The was observed at 516 lg mL-1, whereas maximum
reason might be related to the structural difference of zone of growth inhibition was 24–26 mm [84].
bacterial cell as Gram-positive bacteria posses single Other proposed antibacterial mechanisms of ZnO
cytoplasmic membrane with multilayer of peptido- NPs include direct interaction between ZnO NPs and
glycan polymer and a thicker cell wall, whereas bacterial cells that affect cell membrane permeability
Gram-negative bacteria wall possess two cell mem- following disorganization of the membrane and
branes, an outer membrane and a plasma membrane changing the protein structure [85, 86]. The entry of
with a thin layer of peptidoglycan. Therefore, NPs ZnO NPs as a result of proton motive force and
size can readily pass through the peptidoglycan and uptake of toxic dissolved zinc ions causes oxidative
hence are highly susceptible to damage. stress inside bacterial cell and generation of reactive
The antimicrobial effect of ZnO NPs (50 nm, oxygen species (ROS). The toxicity of ROS to bacteria
spherical) on Campylobacter jejuni, E. coli O15:H7 and is accredited to their high reactivity and oxidizing
Salmonella enteritidis was studied [11]. Bacteria cul- property, the reactive species including hydrogen
tured on agar plates and in broth recorded that the peroxide (H2O2), OH- (hydroxyl radicals) and O2 2
growth of C. Jejuni was completely inhibited at (peroxide) [49, 87]. The toxicity of these species
C0.03 mg mL-1 of ZnO NPs, whereas the concen- includes damage of cellular components such as
tration for growth inhibition in E. coli O157:H7 and S. lipids, DNA and proteins, as a result of their incor-
enteritidis was 0.4 mg mL-1. In this study, it was poration into the bacterial cell membrane. ZnO NPs
observed ZnO NP behaved as a bactericidal but not activate the respiratory enzymes as well, causing
bacteriostatic agent for C. jejuni. inadequate mitochondrial functioning and inhibition
ZnO NPs (60–70 nm) synthesized using Trifolium of cellular metabolism as well as in outflow of cyto-
pratens flower extract and their antibacterial activity plasmic contents ultimately causing cell growth
J Mater Sci

inhibition and or bacterial cell death [88, 89]. A metabolic stages are still needed because physiolog-
schematic representation of interaction between ZnO ical and visual toxicological impacts in higher plants
NPs and bacterial cell has been demonstrated in might not be a sensitive indicator of toxicity. Zn is an
Fig. 4. Uptake of ZnO NPs causes disruption of the essential element used in a majority of biochemical
cell wall and depletion in intracellular content as well and physiological processes within plants [96]. Most
as the disturbance in DNA replication, releasing plants require only minute quantity of Zn
metallic ions and ROS generation in the bacterial cell. (0.05 mg L-1) in soil solution for normal growth;
therefore, higher levels of Zn may lead to phytotox-
icity [57] (Table 4).
Cellular and genotoxicity of zinc oxide The cellular and genotoxicity of ZnO NPs in plants
nanoparticles in plants are related with stimulation of lipid peroxidation and
oxidative stress [97]. Toxicity may also arise due to
The increase in the production of ZnO NPs and their particle dissolution in the nutrient solution and par-
use in diverse areas undoubtedly lead to destructive ticle adhesion onto the root surface, rather than the
impact on the environment and exhibit toxicity in uptake of NPs. Zn2? release by ZnO NPs as a result of
biological species. Studies at proteomic, genomic and

Figure 4 Schematic
presentation of possible
antimicrobial mechanisms of (a)
zinc oxide nanoparticles. a
Attachment of NPs to the cell
surface of bacteria directly. b
Disruption of membrane and
leakage of cytoplasmic
content, inhibition of
respiratory dehydrogenases
and electron transport system,
ATPase complex and
generation of ROS and
reactive species including
hydrogen peroxide (H2O2), (b)
OH- (hydroxyl radicals) and
O2
2 (superoxide), dysfunction
of mitochondria, inhibition of
DNA replication in plasmid,
DNA denaturation.
c Oxidative damage, DNA
damage and other organelle
damage due to excess
production of ROS leading to
cell death.

(c)
 J Mater Sci

Table 4 Negative effects of zinc oxide nanoparticles on plant growth and metabolism

NPs and size Exposure Test plants Effects References

(nm) concentrations

ZnO NPs 500–4000 mg L-1 Prosopisjulifra velutina Increase in CAT activity in roots, stems and leaves; POX [105]
increased only in stems and leaves
ZnO NPs 500 and Brassica oleracea Inhibition of germination and root growth (40.6%) [106]
10–25 nm 1000 lg mL-1
ZnO NPs 20 lg mL-1 Allium cepa Inhibition of root growth [107]
ZnO NPs 2000 lg mL-1 Arachis hypogaea Reduced crop growth and pod yield [62]
ZnO NPs 100 lg mL-1 Allium cepa Mitotic index decreased with increase in pycnotic cells, [17]
cellular dysfunctions
ZnO NPs 10 lg mL-1 Cicer arietinum Decreased root biomass [67]
Zn NPs 2000 mg L-1 Radish, rape, ryegrass, Highly reduced root growth [69]
lettuce, corn,
cucumber
ZnO NPs 1000 mg L-1 (Lollium perenne) Reduced biomass, shrank root tips, epidermis and root caps [10]
9–37 nm ryegrass were broken, highly vacuolated and collapsed cortical cells
ZnO NPs 1000 mg L-1 Cucurbita pepo Reduced biomass (78–90%) [108]
(zucchini)
ZnO NPs 4000 mg L-1 Glycine max (soybean) Decreased root growth [50]
ZnO NPs 2000 mg L-1 Corn, radish, rape, Reduced germination and highly reduced root growth [69]
ryegrass, lettuce,
cucumber
ZnO NPs 1 and 2 g L-1 Sesamum indicum Decreased photosynthetic pigment, biomass and protein [109]
10–15 nm content
ZnO NPs 1 and 2 g L-1 Fagopyrum esculentum Marked decrease in initial growth [110]
ZnO NPs 500 mg L-1 Oryza sativa (rice) Stunted root length and reduction in number of roots [111]
50–100 nm

dissolution or transformation of NPs is possibly Zn2? release by ZnO NPs into the soil may be par-
another reason for toxicity, and it was also hypothe- tially accountable for the lethal effects of ZnO NPs
sized that ZnO NPs became transformed into Zn2? on [102].
the root surface or inside it [45]. These outcomes are Cytotoxicity of ZnO NPs at a concentration of
in accordance with previous reports which concluded 4000 mg L-1 was studied by Lopez-Moreno et al. [50]
that the toxicity of ZnO NPs was solely due to solu- in soybean seedlings. They used random amplified
bilized Zn2? [98–100]. An experiment was conducted polymorphic DNA (RAPD) technique to inspect
by Wang X. et al. [101] to study the toxic effects of genotoxicity by detecting new DNA bands in the
ZnO NPs at a concentration of 300 mg mL-1 on RAPD profile. The toxicity may arise due to the
Arabidopsis. The authors reported the inhibition of interaction of the plant genome with the Zn ions
plant growth resulting in reduced rosette size, gen- released by the ZnO NPs or with the direct interac-
eration of oxidative stress in plant, [50% decrease in tion of DNA with the ZnO NPs, but the results from
chlorophyll a and b which directly led to 50% drop in the XANES study (absence of ZnO NPs in plant tis-
net rate of photosynthesis, transpiration, stomatal sues) failed to determine the precise reason for
conductance in leaf and intercellular CO2 concentra- genotoxic response of ZnO NPs in soybean. In
tion. Authors of this study also observed up to five another study, ZnO NPs at 4000 mg L-1 exhibited
times down-regulation in levels of genes expression toxic effects and decreased seed germination in
of CHLOROPHYLLAOXYGENASE (CAO), CHLOR- tomato, alfalfa, cucumber and soybean. Although
OPHYLLSYNTHASE (CHLG) etc. The exact toxicity reduce seed germination was reported in corn at a
mechanism needs elaboration. It is possible that the concentration of 500 mg L-1 [103]. It is important to
J Mater Sci

note that the majority of plants displayed different plant species exhibit dissimilar behaviour to
detectable signs of reciprocity of NP toxicity speci- ZnO NPs is to be explored. There are limited reports
fying that toxicity was temporary [104]. to describe the biotransformation of NPs in food
crops and their transmission to the subsequent gen-
eration. The potential biomagnification of NPs in the
Conclusion and future aspects food chain is also unidentified. Although this review
summarizes the potential application of ZnO NPs in
This review highlights the possible role of ZnO NPs various agricultural sectors, additional examination
applications in area of agricultural development. In and research are needed to understand the possibil-
the present review, we have discussed the various ities of ZnO NPs application in agriculture.
aspects like eco-friendly biogenic synthesis of ZnO
NPs, mechanism of their uptake, translocation and
accumulation in plants and possible impact of ZnO Acknowledgement
NPs in the agricultural field as nanofertilizer
enhancing the crop productivity. Moreover, protec- The authors are thankful to the University Grant
tion of plants to microbes by the antimicrobial Commission (UGC), New Delhi, India, and Univer-
activity of ZnO NPs has also been discussed. Various sity of Allahabad, India, for providing financial
physiological and biochemical toxicity caused by assistance to Ajey Singh.
varied concentration of ZnO NPs have also been
summarized.
Compliance with ethical standards
NPs synthesized by biological entities are more
Conflict of interest There is no conflict of interest
stable and biocompatible due to the process of coat-
for this manuscript.
ing with biogenic surfactants or capping agents, and
they also show reduced hazardous impacts on the
environment as no toxic chemicals involve in this References
process. The process of uptake, translocation and
accumulation of ZnO NPs in crops is not studied [1] Singh A, Singh NB, Hussain I, Singh H, Singh SC (2015)
adequately as many of the studies have commonly Plant-nanoparticle interaction: an approach to improve
been performed until germination stage only. In this agricultural practices and plant productivity. Int J Pharm Sci
review, we tried to draw an outline for the probable Invent 4(8):25–40
pathways of uptake, translocation and accumulation [2] Khodakovskaya MV, Silva KD, Biris AS, Dervishi E,
of zinc in the form of ZnO NPs and zinc ions in Villagarcia H (2012) Carbon nanotubes induce growth
plants. Despite several beneficial roles of ZnO NPs in enhancement of tobacco cells. ACS Nano 6(3):2128–2135
agriculture sector, the heavy use of ZnO NPs in [3] Auld DS (2001) Zinc coordination sphere in biochemical
various industries certainly leads to negative impact zinc sites. Biometals 14:271–313
on the environment and exhibits toxicity on flora and [4] Rout GR, Das P (2003) Effect of metal toxicity on plant
fauna. growth and metabolism. Agronomie 23:3–11
Although plenty of studies dealing with phyto- [5] Aravind P, Prasad MNV (2004) Zinc protects chloroplasts
toxicity, uptake and accumulation of ZnO NPs have and associated photochemical functions in cadmium
been conducted in the last few years, we are still in exposed Ceratophyllum demersum L., a fresh water
the early stage of this area and various questions macrophyte. Plant Sci 166:1321–1327
need to be answered. The probable connection [6] Hussain I, Singh NB, Singh A, Singh H, Singh SC (2016)
between the different characteristics of NPs like their Green synthesis of nanoparticles and its potential applica-
surface area, size and shape with their performance tion. Biotechnol Lett 38(4):545–560
in biological applications has to be investigated. [7] Singh A, Singh NB, Hussain I, Singh H, Yadav V, Singh
There is need to understand the relationship between SC (2016) Green synthesis of nano zinc oxide and evalu-
plant species and environmental factors with the ation of its impact on germination and metabolic activity of
uptake and accumulation of NPs. Plenty of studies Solanum lycopersicum. J Biotechnol 233:84–94
stated the different resistivity of NPs by different [8] Yadav A, Prasad V, Kathe AA, Raj S, Yadav D, Sun-
plant species, yet the reason of how and why daramoorthy C, Vigneshwaran N (2006) Functional
 J Mater Sci

finishing in cotton fabrics using zinc oxide NPs. Bull Mater [22] Clark J, Macquarrie D (2002) Handbook of green chemistry
Sci 29:641–645 and technology. Blackwell Publishing Ltd., Oxford Press,
[9] Singh NB, Amist N, Yadav K, Singh D, Pandey JK, Singh Oxford
SC (2013) Zinc oxide nanoparticles as fertilizer for the [23] Gnanasangeetha D, Thambavani DS (2013) Biogenic pro-
germination, growth and metabolism of vegetable crops. duction of zinc oxide nanoparticles using Acalypha indica.
J Nanoeng Nanomanufacturing 3:1–12 JCBPSC 4(1):238–246
[10] Lin D, Xing B (2008) Root uptake and phytotoxicity of [24] Agarwal H, Venkat Kumar S, Rajeshkumar S (2017) A
ZnO nanoparticles. Environ Sci Technol 42:5580–5585 review on green synthesis of zinc oxide nanoparticles–an
[11] Xie Y, He Y, Irwin PLI, Jin T, Shi X (2011) Antibacterial eco-friendly approach. Resour Eff Technol. doi:10.1016/j.
activity and mechanism of action against Campylobacter reffit.2017.03.002
jejuni. Appl Environ Microbiol 77(7):2325–2331 [25] Gunalan S, Sivaraj R, Venckatesh R (2011) Green synthesis
[12] Servin A, Elmer W, Mukherjee A, Torre-Roche RD, Hamdi of zinc oxide nanoparticles by Aloe barbadensis miller leaf
H, White JC, Bindraban P, Dimkpa C (2015) A review of extract: structure and optical properties. Mater Res Bull
the use of engineered nanomaterials to suppress plant dis- 46:2560–2566
ease and enhance crop yield. J Nanoparticle Res 17:92 [26] Ramesh P, Rajendran A, Meenakshisundaram M (2014)
[13] Hussain I, Singh NB, Singh A, Singh H, Singh SC, Yadav Green synthesis of zinc oxide nanoparticles using flower
V (2017) Exogenous application of phytosynthesized extract cassia auriculata. J Nanosci Nanotechnol 1:41–45
nanoceria to alleviate ferulic acid stress in Solanum [27] Bala N, Saha S, Chakraborty M, Mati M, Das S, Basu R,
lycopersicum. Sci Hortic 214:158–164 Nandy P (2015) Green synthesis of zinc oxide nanoparti-
[14] Jeevanandam J, Chan YS, Danquah MK (2016) Biosyn- cles using Hibiscus subdariffa leaf extract: effect of tem-
thesis of metal and metal oxide nanoparticles. Chem Bio perature on synthesis, antibacterial activity and anti-
Eng Rev 3:55–67 diabetic. RSC Adv 5:4993
[15] Remedios C, Rosario F, Bastos V (2012) Environmental [28] Singh RP, Shukla VK, Yadav RS, Sharma PK, Singh PK,
nanoparticles interactions with plants: morphological, Pandey AC (2011) Biological approach of zinc oxide
physiological and genotoxic aspects. J Bot. doi:10.1155/ nanoparticles formation and its characterization. Adv Mat
2012/751686 Lett 2(4):313–317
[16] Kumari M, Khan SS, Pakrashi S, Mukherjee A, Chan- [29] Tarafdar JC, Raliya R, Mahawar H, Rathore I (2014)
drasekaran N (2011) Cytogenetic and genotoxic effects of Development of zinc nanofertilizer to enhance crop pro-
zinc oxide NPs on root cells of Allium cepa. J Hazards duction in pearl millet (Pennisetum americanum). Agric
Mater 190:613–621 Res 3(3):257–262
[17] Marcano L, Carruyo I, Del-Campo A, Montiel X (2004) [30] Raliya R, Tarafdar JC (2014) Biosynthesis and characteri-
Cytotoxicity and mode of action of maleic hydrazide in root zation of zinc, magnesium and titanium nanoparticles: an
tips of Allium cepa L. Environ Res 94:221–226 eco-friendly approach. Int Nano Lett 4:93
[18] Ahmed S, Annu Chaudhry SA, Ikram S (2017) A review on [31] Senthilkumar SR, Sivakumar T (2014) Green tea (Camellia
biogenic synthesis of ZnO nanoparticles using plant sinensis) mediated synthesis of zinc oxide (ZnO)
extracts and microbes: a prospect towards green chemistry. nanoparticles and studies on their antimicrobial activities.
J Photochem Photobiol 166:272–284 Int J Pharm Pharm Sci 6(6):461–465
[19] Mittal AK, Chisti Y, Banerjee UC (2013) Synthesis of [32] Devi RS, Gayathri R (2014) Green synthesis of zinc oxide
metallic nanoparticles using plant extracts. Biotechnol Adv nanoparticles by using Hibiscus rosa-sinensis. Int J Curr
31:346–356 Eng Technol 4(4):2444–2446
[20] Jayaseelana C, Rahumana AA, Kirthi AV, Marimuthua S, [33] Samata NA, Nor RM (2013) Sol–gel synthesis of zinc
Santhosh KT, Bagavana A, Gaurav K, Karthik L, Rao KVB oxide nanoparticles using Citrus aurantifolia extracts.
(2012) Novel microbial route to synthesize ZnO nanopar- Ceram Int 39:545–548
ticles using Aeromonas hydrophila and their activity [34] Banumathi B, Malaikozhundan B, Vaseeharan B (2016)
against pathogenic bacteria and fungi. Spectrochim Acta In vitro acaricidal activity of ethnoveterinary plants and
Part A 90:78–84 green synthesis of zinc oxide nanoparticles against Rhipi-
[21] Bhumi G, Savithramma N (2014) Biological synthesis of cephalus (Boophilus) microplus. Vet Parasitol 216:93–100
zinc oxide NPs from Catharanthus roseus (L.) G. Don. [35] Vishwakarma K (2011) Green synthesis of ZnO nanopar-
Leaf extract and validation for antibacterial activity. Int J ticles using Abrus precatorius seeds extract and their
Drug Dev Res 6(1):208–214
J Mater Sci

characterization. PhD thesis, National institute of technol- [50] Lopez-Moreno ML, De La Rosa G, Hernandez-Viezcas JA,
ogy Rourkela Castillo-Michel H, Botez CE, Peralta-Videa JR, Gardea-
[36] Sarkar J, Ghosh M, Mukherjee A, Chattopadhyay D, Torresdey JL (2010) Evidence of the differential biotrans-
Acharya K (2014) Biosynthesis and safety evaluation of formation and genotoxicity of ZnO and CeO2 NPs on
ZnO nanoparticles. Bioprocess Biosyst Eng 37:165–171 soybean (Glycine max) plants. Environ Sci Technol
[37] Fu L, Fu Z (2015) Plectranthus amboinicus leaf extract- 44:7315–7320
assisted biosynthesis of ZnO nanoparticles and their pho- [51] Scheckel KG, Luxton TP, El Badawy AM, Impellitteri CA,
tocatalytic activity. Ceram Int 41:2492–2496 Tolaymat TM (2010) Synchrotron speciation of silver and
[38] Bhuyan T, Mishra K, Khanuja M, Prasad R, Varma A zinc oxide nanoparticles aged in a kaolin suspension.
(2015) Biosynthesis of zinc oxide nanoparticles from Environ Sci Technol 44(4):1307–1312
Azadirachta indica for antibacterial and photocatalytic [52] Reed RB, Ladner DA, Higgins CP, Westerhoff P, Ranville
applications. Mater Sci Semicond Process 32:55–61 JF (2012) Solubility of nano-zinc oxide in environmentally
[39] Yedurkar S, Maurya C, Mahanwar P (2016) Biosynthesis of and biologically important matrices. Environ Toxicol Chem
zinc oxide nanoparticles using Ixora coccinea leaf extract-A 31(1):93–99
green approach. Open J Synth Theory Appl 5:1–14 [53] Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ
[40] Balusamy B, Kandhasamy YG, Senthamizhan A, Chan- (1999) Zinc ligands 471 in the metal hyperaccumulator
drasekaran G, Subramanian MS, Tirukalikundram K (2012) Thlaspica erulescens as determined using X-ray absorption
Characterization and bacterial toxicity of lanthanum oxide spectroscopy. Environ Sci Technol 33(5):713–717
bulk and nanoparticles. J Rare Earth 30:1298–1302 [54] Jitao LV, Zhang S, Luo L, Zhang J, Yang K, Christied P
[41] Narendhran S, Shivraj R (2016) Biogenic ZnO NPs synthe- (2015) Accumulation, speciation and uptake pathway of
sised using L. aculeate leaf extract and there antifungal activity ZnO nanoparticles in maize. Environ Sci Nano 2:68
against plant fungal pathogens. Bull Mater Sci 39(1):1–5 [55] Zhao LJ, Peralta-Videa JR, Ren MH, Varela-Ramirez A,
[42] Nagarajan S, Kuppusamy A (2013) Extracellular synthesis Hernandez-Viezcas CQ, Li JA, Aguilera RJ, Gardea-Tor-
of zinc oxide nanoparticle using seaweeds of gulf of resdey JL (2012) Transport of zinc in a sandy loam soil
Mannar, India. J Nanobiotechnol 11:39 treated with ZnO NPs and uptake by corn plants: Electron
[43] Rajiv P, Rajeshwari S, Venckatesh R (2013) Bio-fabrication microprobe and confocal microscopy studies. Chem Eng J
of zinc oxide nanoparticles using leaf extract of Parthe- 184:1–8
nium hysterophorus L. and its size-dependent antifungal [56] Alloway B, Graham R, Stacey S (2008) Micronutrient
activity against plant fungal pathogens. Spectrochim Acta deficiencies in Australian field crops: In Micronutrient
Part A 112:384–387 deficiencies in global crop production. Springer Nether-
[44] Yu H, Ming H, Gong J, Li H, Huang H, Pan K, Liu Y, Kang lands, pp 63–92
Z, Wei J, Wang D (2013) Facile synthesis of Au/ZnO [57] Liu R, Lal R (2015) Potentials of engineered nanoparticles
nanoparticles and their enhanced photocatalytic activity for as fertilizers for increasing agronomic productions. Sci
hydroxylation of benzene. Bull Mater Sci 36:367–372 Total Environ 514:131–139
[45] Wang P, Menzies NW, Lombi E, McKenna BA, Johan- [58] Milani N, McLaughlin MJ, Stacey SP, Kirby JK, Het-
nessen B, Glover CJ, Kappen P, Kopittke PM (2013) Fate tiarachchi GM, Beak DG, Cornelis G (2012) Dissolution
of ZnO nanoparticles in soils and cowpea (Vigna unguic- kinetics of macronutrient fertilizers coated with manufac-
ulata). Environ Sci Technol 47:13822–13830 tured zinc oxide nanoparticles. J Agric Food Chem
[46] Handy RD, Owen R, Valsami-Jones E (2008) The eco- 60(16):3991–3998
toxicology of nanoparticles and nanomaterials: current [59] Raliya R, Nair R, Chavalmane S, Wangab WN, Biswas P
status, knowledge gaps, challenges, and future needs. (2015) Mechanistic evaluation of translocation and physi-
Ecotoxicology 17(5):315–325 ological impact of titanium dioxide and zinc oxide
[47] Biswas P, Wu CY (2005) Critical review: nanoparticles and nanoparticles on the tomato (Solanum lycopersicum L.)
the environment. J Air Waste Manag Assoc 55(6):708–746 plant. Metallomics 7:1584–1594
[48] Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, [60] Watson JL, Fang T, Dimpka CO, Britt DW, McLean JE,
Kumar DS (2010) Nanoparticulate material delivery to Jacobson A, Anderson AJ (2015) The phytotoxicity of ZnO
plants. Plant Sci 179:154–163 nanoparticles on wheat varies with soil properties.
[49] Klaine SJ, Alvarez PJ, Batley GE et al (2008) Nanomate- Biometals 28(1):101–112
rials in the environment: behaviour, fate, bioavailability, [61] Raliya R, Tarafdar JC (2013) ZnO nanoparticle biosyn-
and effects. Environ Toxicol Chem 27(9):1825–1851 thesis and its effect on phosphorous-mobilizing enzyme
 J Mater Sci

secretion and gum contents in cluster bean (Cyamopsis mitigation of salinity stress in lupine (Lupinus termis)
tetragonoloba L.). Agric Res 2:48–57 plants. J Plant Growth Regul 36(1):60–70
[62] Prasad TNVKV, Sudhakar P, Sreenivasulu Y, Latha P, [74] Lawre S, Raskar S (2014) Influence of zinc oxide
Munaswamy V, Raja Reddy K, Sreeprasad TS, Sajanlal PR, nanoparticles on growth, flowering and seed productivity in
Pradeep T (2012) Effect of nanoscale zinc oxide particles onion. Int J Curr Microbiol Appl Sci 3(7):874–881
on the germination, growth and yield of peanut. J Plant [75] Zafar H, Ali A, Ali JS, Haq IU, Zia M (2016) Effect of ZnO
Nutr 35(6):905–927 nanoparticles on Brassica nigra seedlings and stem
[63] Ates M, Daniels J, Arslan Z, Farah IO, Rivera HF (2013) explants: growth dynamics and antioxidative response.
Comparative evaluation of impact of Zn and ZnO Front Plant Sci 7:535. doi:10.3389/fpls.2016.00535
nanoparticles on brine shrimp (Artemia salina) larvae: [76] Vigneshwaran N, Kathe AA, Varadarajan PV, Nachane RP,
effects of particle size and solubility on toxicity. Environ sci Balasubramanya RH (2007) Silverprotein (coreshell) NP
Processes Impacts 1:10. doi:10.1039/c2em30540b production using spent mushroom substrate. Langmuir
[64] Peng C, Zhang W, Gao H, Li Y, Tong X, Li K, Zhu X, 23:7113–7117
Wang Y, Chen Y (2017) Behavior and potential impacts of [77] Sirelkhatim A, Mahmud S, Seeni A, Haida N, Kaus M, Ann
metal-based engineered nanoparticles in aquatic environ- Ling Chuo, Bakhori SKM, Hasan H, Mohamad D (2015)
ments. Nanomaterials 7(1):21 Review on Zinc oxide nanoparticles: antibacterial activity
[65] Misra SK, Nuseibeh S, Dybowska A, Berhanu D, Tetley and toxicity mechanism. Nano-micro Lett 7(3):219–242
TD, Valsami-Jones E (2014) Comparative study using [78] Dimkpa CO, Mclean JE, Latta DE, Manangon E, Britt DW,
spheres, rods and spindle-shaped nanoplatelets on disper- Johnson WP, Boyanov MI, Anderson AJ (2012) CuO and
sion stability, dissolution and toxicity of CuO nanomateri- ZnO nanoparticles: phytotoxicity, metal speciation, and
als. Nanotoxicology 8:422–432 induction of oxidative stress in sand-grown wheat.
[66] Zhao LJ, Peralta-Videa JR, Rico CM, Hernandez-Viezcas J Nanoparticle Res 14:112
JA, Sun Y, Niu G, Servin A, Nunez JE, Duarte-Gardea M, [79] Kumar SS, Venkateswarlu P, Rao VR, Rao GN (2013)
Gardea-Torresdey JL (2014) CeO2 and ZnO nanoparticles Synthesis, characterization and optical properties of zinc
change the nutritional quality of cucumber (Cucumis sati- oxide nanoparticles. Int Nano Lett 3:1–6
vus). J Agric Food Chem 62:2752–2759 [80] Kaur P, Thakur R, Kumar S, Dilbaghi N (2011) Interaction
[67] Pradhan S, Patra P, Das S, Chandra S, Mitra S, Dey KK, of ZnO nanoparticles with food borne pathogens Escher-
Akbar S, Palit P, Goswami A (2013) Photochemical mod- ichia coli DH5a and Staphylococcus aureus 5021 and their
ulation of biosafe manganese nanoparticles on vigna radi- bactericidal efficacy, In International conference on
ata: a detailed molecular, biochemical and biophysical advances in condensed and nano materials (ICACNM-
study. Environ Sci Technol 47(22):13122–13131 2011): AIP proceedings, Chandigarh, India pp 153
[68] Mahajan P, Dhoke SK, Khanna AS, Tarafdar JC (2011) [81] Narayanan P, Wilson WS, Abraham AT, Sevanan M (2012)
Effect of nano-ZnO on growth of mung bean (Vigna Synthesis, characterization, and antimicrobial activity of
radiata) and chickpea (Cicer arietinum) seedlings using zinc oxide nanoparticles against human pathogens.
plant agar method. Appl Biol Res 13:54–61 BioNanoScience 2(4):329–335
[69] Lin D, Xing B (2007) Phytotoxicity of nanoparticles: [82] Azeredo HD (2013) Antimicrobial nanostructures in food
inhibition of seed germination and root growth. Environ packaging. Trends Food Sci Technol 30(1):56–69
Pollut 150:243–250 [83] Soares NFF, Silva CAS, Santiago-Silva P, Espitia PJP,
[70] Burman U, Saini M, Kumar P (2013) Effect of zinc oxide Goncalves MPJC, Lopez MJG, Miltz J, Cerqueira MA,
nanoparticles on growth and antioxidant system of chickpea Vicente AA, Teixeira J, Silva WA, Botrel DA (2009) Active
seedlings. Toxicol Environ Chem 95(4):605–612 and intelligent packaging for milk and milk products. In:
[71] Dhoke SK, Mahajan P, Kamble R, Khanna A (2013) Effect Coimbra JSR, Teixeira JA (eds) Engineering aspects of
of nanoparticles suspension on the growth of mung (Vigna milk and dairy products. CRC Press Taylor & Francis
radiata) seedlings by foliar spray method. Nanotechnol group, New York, pp 155–174. doi:10.1201/
Dev 3(1):e1 9781420090390-c8
[72] Taheri M, Qarache HA, Qarache AA, Yoosefi M (2015) [84] Dobrucka R, Dugaszewska J (2016) Biosynthesis and
The effects of zinc-oxide nanoparticles on growth param- antibacterial activity of ZnO nanoparticles using Trifolium
eters of corn (SC704). STEM Fellowsh J 1(2):17–20 pratense flower Extract. Saudi J Biol Sci 23(4):517–523
[73] Latef AAHA, Alhmad MFA, Abdelfattah KE (2017) The [85] Premanathan M, Karthikeyan K, Jeyasubramanian K,
possible roles of priming with ZnO nanoparticles in Manivannan G (2011) Nanomed: selective toxicity of ZnO
J Mater Sci

nanoparticles toward Gram-positive bacteria and cancer [99] Miao AJ, Zhang XY, Luo Z, Chen CS, Chin WC, Santschi
cells by apoptosis through lipid peroxidation. Nanomedi- PH, Quigg A (2010) Zinc oxide engineered nanoparticles:
cine 7:184–192 dissolution and toxicity to marine phytoplankton. Environ
[86] Vani C, Sergin GK, Annamalai A (2011) A study on the Toxicol Chem 29(12):2814–2822
effect of zinc oxide nanoparticle in staphylococcus aureus. [100] Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of
Int J Pharma Bio Sci 2(4):326–335 manufactured ZnO nanoparticles–a review. Environ Pollut
[87] Padmavathy N, Vijayaraghavan RR (2008) Enhanced 172:76–85
bioactivity of ZnO nanoparticles-an antimicrobial study. Sci [101] Wang X, Yang X, Chen S, Li Q, Wang W, Hou C, Gao X,
Technol Adv Mater 9:035004 Wang L, Wang S (2016) Zinc oxide nanoparticles affect
[88] Kairyte K, Kadys A, Luksiene Z (2013) Antimicrobial and biomass accumulation and photosynthesis in Arabidopsis.
antifungal activity of photoactivated ZnO nanoparticles in Front plant Sci 6:1243
suspension. J Photochem Photobiol B 128:78–84 [102] Cornelis G, Hund-Rinke K, Kuhlbusch T, vandenBrink N,
[89] Sharma D, Rajput J, Kaith BS, Kaur M, Sharma S (2010) Nickel C (2014) Fate and bioavailability of engineered
Synthesis of ZnO nanoparticles and study of their nanoparticles in soils: a review. Crit Rev Env Sci Technol
antibacterial and antifungal properties. Thin Solid Films 44:2720–2764
519(3):1224–1229 [103] de la Rosa G, Lopez-Moreno ML, De Haro D, Botez CE,
[90] Molina MA, Ramos JL, Espinosa-Urgel M (2006) A two- Peralta-Videa JR, Gardea-Torresdey J (2013) Effects of
partner secretion system is involved in seed and root col- ZnO nanoparticles in alfalfa, tomato, and cucumber at the
onization and iron uptake by Pseudomonas putida KT2440. germination stage: root development and X-ray absorption
Environ Microbiol 8(4):639–647 spectroscopy studies. Pure Appl Chem 85(12):2161–2174
[91] Wani AH, Shah MA (2012) A unique and profound effect [104] Kumari M, Khan SS, Pakrashi S, Mukherjee A, Chan-
of MgO and ZnO nanoparticles on some plant pathogenic drasekaran N (2011) Cytogenetic and genotoxic effects of
fungi. J appl Pharm Sci 2(3):40–44 zinc oxide NPs on root cells of Allium cepa. J Hazard
[92] Dimpka CO, McLean JE, Britt DW, Anderson AJ (2013) Mater 190(1–3):613–621
Antifungal activity of ZnO nanoparticles and their inter- [105] Hernandez-Viezcas JA, Castillo-Michael H, Servin AD,
active effect with a biocontrol bacterium on growth Peralta-Videa JR, Gardea-Torresdey JL (2011) Spectroscopic
antagonism of the plant pathogen Fusarium graminearum. verification of zinc absorption and distribution in the desert
Biometals 26(6):913–924 plant Prosopisjuliflora velutina (velvet mesquite) treated
[93] He L, Liu Y, Mustapa A, Lin M (2011) Antifungal activity with ZnO nanoparticles. Chem Eng J 170(1–3):346–352
of zinc oxide nanoparticles against Botrytis cinerea and [106] Pokhrel LR, Dubey B (2013) Evaluation of developmental
Penicillium expansum. Microbiol Res 166(3):207–215 responses of two crop plants exposed to silver and zinc
[94] Rispail N et al (2014) Quantum dot and superparamagnetic oxide nanoparticles. Sci Total Environ 452–453:321–332
nanoparticle interaction with pathogenic fungi: internal- [107] Ghodake G, Seo YD, Lee DS (2011) Hazardous phytotoxic
ization and toxicity profile. ACS Appl Mater Interfaces nature of cobalt and zinc oxide nanoparticles assessed using
6(12):9100–9110 Allium cepa. J Hazards Mater 186:952–955
[95] Mirhosseini M, Barzegari Firouzabadi F (2015) Reduction [108] Stampoulis D, Sinha SK, White JC (2009) Assay-depen-
of Listeria monocytogenes and Bacillus cereus in Milk by dent phytotoxicity of nanoparticles to plants. Environ Sci
Zinc oxide Nanoparticles. Iran J Pathol 10(2):97–104 Technol 43(24):9473–9479
[96] Li Z, Yang R, Yu M, Bai F, Li C, Wang ZL (2008) Cellular [109] Narendhran S, Rajiv P, Sivaraj R (2016) Toxicity of ZnO
level biocompatibility and biosafety of ZnO nanowires. nanoparticles on germinating Sesamum indicum (Co-1)
J Phys Chem C 112(51):20114–20117 and their antibacterial activity. Bull Mater Sci
[97] Han D, Tian Y, Zhang T, Ren G, Yang Z (2011) Nano-zinc 39(2):415–421
oxide damages spatial cognition capability via over-en- [110] Lee S, Kim S, Kim S, Lee I (2013) Assessment of phyto-
hanced long-term potentiation in hippocampus of Wistar toxicity of ZnO NPs on a medicinal plant Fagopyrum
rats. Int J Nanomedicine 6:1453–1461 esculentum. Environ Sci Pollut Res Int 20:848–854
[98] Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, [111] Boonyanitipong P, Kumar P, Kositsup B, Baruah S, Dutta J
Casey PS (2007) Comparative toxicity of nanoparticulate (2011) Effects of zinc oxide nanoparticles on roots of rice
ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga Oryza Sativa L. In International conference on environ-
(Pseudokirchneriella subcapitata): the importance of parti- ment and bioscience IPCBEE. 21st edn. IACSIT Press,
cle solubility. Environ Sci Technol 41(24):8484–8490 Singapore